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Natural or light-induced pigment accumulation in grain amaranths coincides with enhanced resistance against insect herbivory

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Abstract

Main conclusion

Increased resistance to insect herbivory in grain amaranth plants is associated with increased betalain pigmentation, either naturally acquired or accumulated in response to blue-red light irradiation .

Abstract

Betalains are water-soluble pigments characteristic of plants of the Caryophyllales order. Their abiotic stress-induced accumulation is believed to protect against oxidative damage, while their defensive function against biotic aggressors is scarce. A previous observation of induced betalain-biosynthetic gene expression in stressed grain amaranth plants led to the proposal that these pigments play a defensive role against insect herbivory. This study provided further support for this premise. First, a comparison of “green” and “red” Amaranthus cruentus phenotypes showed that the latter suffered less insect herbivory damage. Coincidentally, growth and vitality of Manduca sexta larvae were more severely affected when fed on red-leafed A. cruentus plants or on an artificial diet supplemented with red-leaf pigment extracts. Second, the exposure of A. cruentus and A. caudatus plants, having contrasting pigmentation phenotypes, to light enriched in the blue and red wavelength spectra led to pigment accumulation throughout the plant and to increased resistance to insect herbivory. These events were accompanied by the induced expression of known betalain-biosynthetic genes, including uncharacterized DODA genes believed to participate in this biosynthetic pathway in a still undefined way. Finally, transient co-expression of different combinations of betalain-biosynthetic genes in Nicotiana benthamiana led to detectable accumulation of betalamic acid and betanidin. This outcome supported the participation of certain AhDODA and other genes in the grain amaranth betalain-biosynthetic pathway.

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Fig. 1

adapted from Polturak et al. 2018)

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

BR:

Blue/red

cyclo-DOPA:

Cyclodihydroxyphenylalanine

DODA:

DOPA 4,5-dioxygenase

L-DOPA:

L-Dihydroxyphenylalanine

UPLC-MS:

Ultra-performance liquid chromatography system coupled to mass-spectrometry

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Acknowledgements

The authors wish to thank Dr. Jorge Ibarra Rendón and Javier Lúevano Borroel from Cinvestav, unidad Irapuato for their generous gift of the M. sexta larvae utilized for the insect herbivory experiments.

Funding

CPN was supported by a postgraduate scholarship granted by The National Council for Science and Technology (CONACYT, México), Code No. 268236.

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Authors and Affiliations

  1. Department of Biotechnology and Biochemistry, Centro de Investigación y de Estudios Avanzados del IPN, Unidad Irapuato, Kilómetro 9.6 Libramiento Norte Carretera Irapuato-León, CP, 36821, Irapuato, Guanajuato, México

    Claudia Portillo-Nava, Armando Guerrero-Rangel, Norma Martínez-Gallardo, Lino Sánchez-Segura & John Délano-Frier

  2. Metabolomics Laboratory, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Unidad de Genómica Avanzada, Kilómetro 9.6 Libramiento Norte Carretera Irapuato-León, CP, 36821, Irapuato, Guanajuato, México

    Moisés Guerrero-Esperanza, Paulina Guevara-Domínguez & José Ordaz-Ortiz

  3. Escuela Nacional de Ciencias Biológicas del Instituto Politécnico Nacional, Unidad Profesional Lázaro Cárdenas, Prolongación de Carpio y Plan de Ayala S/N,Col. Santo Tomás, CDMX, CP, 11340, Alcaldía Miguel Hidalgo, México

    Cecilia Nava-Sandoval

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  1. Claudia Portillo-Nava
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Portillo-Nava, C., Guerrero-Esperanza, M., Guerrero-Rangel, A. et al. Natural or light-induced pigment accumulation in grain amaranths coincides with enhanced resistance against insect herbivory. Planta 254, 101 (2021). https://doi.org/10.1007/s00425-021-03757-3

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